Bottom Line:
These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens.At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits.Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

Affiliation: Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.

ABSTRACTIron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth's early history. Before the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled Earth's early biosphere providing energy to drive microbial growth and evolution over billions of years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving models for early biological production untested and imperative ecological context for the evolution of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

Mentions:
To directly test for photoferrotrophic activity in KB, we conducted a suite of incubation experiments in which rates of Fe(II) oxidation were measured over time. In the first set of experiments, we incubated water samples between 10.5 and 11.3 m by suspending triplicate glass incubation vessels directly in the water column so that the microbial community would experience near in situ light conditions with an average diel illumination of 0.6 μE m−2 s−1 and a mid-day maximum of 3.2 μE m−2 s−1. We measured light-dependant Fe(II) oxidation rates up to 100 μmol Fe l−1 d−1, demonstrating active photoferrotrophic activity in the KB chemocline (Fig. 3a). At 8 × 107 GSB cells l−1, cell specific Fe oxidation rates are up to 1.25 pmol cell−1 d−1. Depth-integrated Fe(II) oxidation rates of 36.8 mmol Fe m−2 d−1 were computed by taking the mean of the measured rates between 10.5 and 11.3 m, and multiplying by the 0.8 m interval. This Fe(II) oxidation could drive carbon (C) fixation at rates of 9.2 mmol C m−2 d−1 based on the expected (4:1) relationship between Fe oxidation to C-fixation during photoferrotrophy14; nearly the same rate (9 mmol C m−2 d−1) as measured directly by 13C labelling experiments. Rates of photosynthetic C fixation in the chemocline were up to 28% of the production in the oxic suface waters (32 mmol C m−2 d−1). While cyanobacteria and GSB co-occur in the chemocline, low average Chl a concentrations (ca. 1.1 μg l−1) and BChl e:Chl a ratios of more than about 100 highlight the dominance of GSB in the ferruginous waters. The importance of photoferrotrophy in the chemocline of KB is underscored by mass balance on the stable C isotope composition of particulate organic matter. Using a simple isotope-mixing model (Supplementary Information) we estimated that 74% ± 13% of the particulate organic carbon pool in the chemocline is derived through anoxygenic photosynthesis by GSB, with a maximum (89%) at 11.25 m. This mass balance reveals that GSB constituted 208 mmol m−2 biomass, which together with the light-dependent C fixation rates translates to a GSB biomass turnover time of 23 d.

Mentions:
To directly test for photoferrotrophic activity in KB, we conducted a suite of incubation experiments in which rates of Fe(II) oxidation were measured over time. In the first set of experiments, we incubated water samples between 10.5 and 11.3 m by suspending triplicate glass incubation vessels directly in the water column so that the microbial community would experience near in situ light conditions with an average diel illumination of 0.6 μE m−2 s−1 and a mid-day maximum of 3.2 μE m−2 s−1. We measured light-dependant Fe(II) oxidation rates up to 100 μmol Fe l−1 d−1, demonstrating active photoferrotrophic activity in the KB chemocline (Fig. 3a). At 8 × 107 GSB cells l−1, cell specific Fe oxidation rates are up to 1.25 pmol cell−1 d−1. Depth-integrated Fe(II) oxidation rates of 36.8 mmol Fe m−2 d−1 were computed by taking the mean of the measured rates between 10.5 and 11.3 m, and multiplying by the 0.8 m interval. This Fe(II) oxidation could drive carbon (C) fixation at rates of 9.2 mmol C m−2 d−1 based on the expected (4:1) relationship between Fe oxidation to C-fixation during photoferrotrophy14; nearly the same rate (9 mmol C m−2 d−1) as measured directly by 13C labelling experiments. Rates of photosynthetic C fixation in the chemocline were up to 28% of the production in the oxic suface waters (32 mmol C m−2 d−1). While cyanobacteria and GSB co-occur in the chemocline, low average Chl a concentrations (ca. 1.1 μg l−1) and BChl e:Chl a ratios of more than about 100 highlight the dominance of GSB in the ferruginous waters. The importance of photoferrotrophy in the chemocline of KB is underscored by mass balance on the stable C isotope composition of particulate organic matter. Using a simple isotope-mixing model (Supplementary Information) we estimated that 74% ± 13% of the particulate organic carbon pool in the chemocline is derived through anoxygenic photosynthesis by GSB, with a maximum (89%) at 11.25 m. This mass balance reveals that GSB constituted 208 mmol m−2 biomass, which together with the light-dependent C fixation rates translates to a GSB biomass turnover time of 23 d.

Bottom Line:
These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens.At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits.Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

Affiliation:
Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.

ABSTRACTIron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth's early history. Before the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled Earth's early biosphere providing energy to drive microbial growth and evolution over billions of years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving models for early biological production untested and imperative ecological context for the evolution of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.